Invertebrate Zoology, 2014, 11(2): 293–314 © INVERTEBRATE ZOOLOGY, 2014

Tube morphology, ultrastructures and mineralogy in recent Spirorbinae (Annelida: Polychaeta: ). I. General introduction. Tribe Paralaeospirini

A.P. Ippolitov1, A.V. Rzhavsky2

1 Geological Institute of Russian Academy of Sciences (GIN RAS), 7 Pyzhevskiy per., Moscow, Russia, 119017, e-mail: [email protected] 2 A.N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences (IPEE RAS), 33 Leninskiy prosp., Moscow, Russia, 119071, e-mail: [email protected]

ABSTRACT: This report is the first part of a series of papers that provide an overview of tube morphology, mineralogy, and ultrastructures within the subfamily Spirorbinae, includ- ing the discussion of taxonomic and phylogenetic significance of the tube features. This paper reviews published data on the subject and provides descriptions of ultrastructure and mineralogy for the tribe Paralaeospirini Knight-Jones, 1978. The species of the tribe have uniformly simple calcitic unilayered tubes of the same irregularly oriented prismatic (IOP) ultrastructural type, which is regarded as plesiomorphic among serpulids. How to cite this article: Ippolitov A.P., Rzhavsky A.V. 2014. Tube morphology, ultrastruc- tures and mineralogy in recent Spirorbinae (Annelida: Polychaeta: Serpulidae). I. General introduction. Tribe Paralaeospirini // Invert. Zool. Vol. 11. No. 2.

KEY WORDS: Tube ultrastructures, tube morphology, tube mineralogy, scanning electron microscopy, X-ray diffraction analysis, Spirorbinae, Paralaeospirini.

Морфология, ультраструктуры и минералогия трубок современных Spirorbinae (Annelida: Polychaeta: Serpulidae). I. Общее введение. Материал и методы. Триба Paralaeospirini

А.П. Ипполитов1, А.В. Ржавский2

1 Геологический институт РАН, Пыжевский пер. 7, Москва, Россия, 119017, e-mail: [email protected] 2 Институт проблем экологии и эволюции им. А.Н. Северцова РАН, Ленинский пр. 33, Москва, Россия, 119071, e-mail: [email protected]

РЕЗЮМЕ: В настоящей серии статей приводится обзор морфологического, ультра- структурного и минералогического разнообразия трубок подсемейства Spirorbinae, а также обсуждается возможное таксономическое и филогенетическое значения признаков трубок. В первой части серии мы приводим обзор опубликованных данных, а также даем описания морфологии трубок, их ультраструктур и минерало- гии для трибы Paralaeospirini Knight-Jones, 1978. Установлено, что виды, представ- ляющие трибу, имеют однослойные кальцитовые трубки из хаотически ориентиро- ванных призматических кристаллов. Данный тип строения трубок интерпретируется как архаичный для серпулид. 294 A.P. Ippolitov, A.V. Rzhavsky

Как цитировать эту статью: Ippolitov A.P., Rzhavsky A.V. 2014. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae (Annelida: Polychaeta: Serpulidae). I. General introduction. Tribe Paralaeospirini // Invert. Zool. Vol. 11. No. 2.

КЛЮЧЕВЫЕ СЛОВА: Ультраструктура трубок, морфология трубок, минералогия трубок, сканирующая электронная микроскопия, рентгенодифракционный анализ, Spirorbinae, Paralaeospirini.

Introduction 1981; Jäger, 1983, 1993) that spirorbins are an ancient group dating back to the Subfamily Spirorbinae of the family Serpul- period (~445–485 Ma1), true spirorbins seem to idae Rafinesque, 1815 is a widely distributed appear from the Latest or Earliest Cre- group of small marine that inhabit taceous (~145 Ma: see Taylor, Vinn, 2006). calcareous tubes tightly coiled into spirals and Non-spirorbin nature of more ancient Paleozoic attached to a variety of substrata. Recent spirorb- to Early Mesozoic tubes, which look undistin- ins have world-wide distribution ranging from guishable from spirorbins by external morphol- littoral to abyssal depths, but are most common- ogy, was recognized by morphology of their ly found in the sublittoral zone. internal septae (Burchette, Riding, 1977), study Family Serpulidae was traditionally subdi- of tube microstructures (Burchette, Riding, 1977; vided into subfamilies Spirorbinae Chamberlin, Weedon, 1990, 1991) and comparison with 1919, Serpulinae Rafinesque, 1815, and Filog- those of Recent forms (Weedon, 1994; Taylor, raninae Rioja (1923) (e.g., Rioja, 1923; Fauvel, Vinn, 2006). These ancient fossils are now 1927). Pillai (1970) elevated Spirorbinae to the placed not only outside Spirorbinae, but also family status, which was accepted both in Re- outside the phylum Annelida (see Vinn, Taylor, cent and fossil (e.g., Knight-Jones P., 2007). Fordy M., 1979; Lommerzheim, 1981; Jäger, During the period (145–66 Ma), 1993, 2005; Rzhavsky, 1994). Later numerous coiled serpulids attributed to spirorbins were authors (e.g., ten Hove, 1984; Smith, 1991, represented mostly by the large-sized and pecu- Kupriyanova, 2003; Kupriyanova et al., 2006; liar Neomicrorbis Rovereto, 1903. The Lehrke et al., 2007), based on the results of most ancient finds of this genus are described phylogenetic analyses of morphological and from the Late Barremian (~128 Ma; Jäger, 2011), molecular data, concluded that spirorbins con- but finds of somewhat similar tubes are more stitute a monophyletic group nested inside the ancient (see Jäger, 1983, 1993, 2011). Neomi- Serpulidae. Therefore, the rank of the spiror- crorbis tubes, unlike most spirorbins, are coiled bids was lowered to the subfamily and all former in any direction and often have characteristic subfamilies established within Spirorbidae (see sculpture of numerous rows of tiny tubercules. Knight-Jones P., Fordy, 1979) became tribes Information on the body morphology available (Rzhavsky et al., 2013). The current state of from the only known Recent species Neomi- classification of Spirorbinae that includes 6 crorbis azoricus Zibrowius, 1972 (Zibrowius, tribes, 24 genera, and 131 (135?) species is 1972; Hove, Kupriyanova, 2006) does not al- summarized in Table 1. low to make a certain conclusion about its phylogenetic position inside Serpulidae. Spirorbin fossil record. Spirorbins calcare- Unquestionable spirorbin species that ap- ous tubes have a good potential to fossilize, peared in the middle of the Early Cretaceous providing a basis for substantial fossil record for these polychaetes. Contrary to the long-held 1 Absolute ages are provided according to official site of the International Commission of Stratigraphy view (e.g., Goldfuss, 1831; Zittel, 1880; How- (www.stratigraphy.org/GSSP/index.html), accessed 01- ell, 1962; Pillai, 1970; Lommerzheim, 1979, 03-2013. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 295

Table 1. Compiled classification of Recent spirorbins, including tribes, genera and number of valid spe- cies. Some species of uncertain generic affinity are not considered in the table. Таблица 1. Классификация современных спирорбин (трибы, рода и число валидных видов). Некоторые виды неясной родовой принадлежности не учтены.

Number of Tribe Genus species Paralaeospirini Knight-Jones, 1978 Paralaeospira Caullery et Mesnil, 1897 10 Anomalorbis Vine, 1972 1 Incertae sedis (Paralaeospirini?) Crozetospira Rzhavsky, 1997 1 Spirorbini Chamberlin, 1919 Daudin, 1800 15 Circeis Saint-Joseph, 1894 6 Circeini Knight-Jones, 1978 Paradexiospira Caullery et Mesnil, 1897 3(4?) Eulaeospira Pillai, 1970 2 Helicosiphon Gravier, 1907 1 Knightjonesia Pillai, 2009 1 Romanchellini Knight-Jones, 1978 Metalaeospira Pillai, 1970 4 Protolaeospira Pixell, 1912 12 Romanchella Caullery et Mesnil, 1897 8 Janua Saint-Joseph, 1894 1 Leodora Saint-Joseph, 1894 1 Januini Knight-Jones, 1978 Neodexiospira Pillai, 1970 10(11?) Pillaiospira Knight-Jones, 1973 3 Amplicaria Knight-Jones, 1984 1 Bushiella Knight-Jones, 1973 13(14?) Nidificaria Knight-Jones, 1984 8 Pileolariini Knight-Jones, 1978 Pileolaria Claparède, 1868 21(22?) Protoleodora Pillai, 1970 4 Simplaria Knight-Jones, 1984 3 Vinearia Knight-Jones, 1984 3 Incertae sedis Neomicrorbis Rovereto, 1903 1

(Late Barremian; ~126 Ma; Jäger, 2011) are phology is less uniform and better studied to represented by tubes, morphologically compa- allow classification of fossil species within Re- rable with those of extant species of genera cent genera (see Jäger, 1993, 2005), while for Pileolaria and Neodexiospira. From the latest spirorbins determination of generic affinity based Cretaceous (Late Maastrichtian; ~66 Ma) spir- on empty tubes remains problematic. As a re- orbins became a very common element of en- sult, despite existing fossil record, zoologists crusting communities (e.g., Jäger, 1983, 1993). still have no reliable paleontological data for Younger Paleogene (Paleocene, 62–59 Ma; Lom- understanding evolutionary history of the group, merzheim, 1981) and especially Neogene (like while paleontologists are restricted in their geo- Badenian, 16–13 Ma; Radwańska, 1994, etc.) logical, paleoecological, and biogeographical sediments already contain highly diversified interpretations because no direct comparison of spirorbin communities similar to Recent ones. fossils with Recent taxa is possible. If determi- Classification of Recent spirorbins is cur- nations of fossil spirorbin tubes from Late Bar- rently built around the methods of embryos remian (~126 Ma) are correct, this means that incubation, as well as body and chaetal charac- two of the Recent tribes characterized by com- ters, while tubes are mostly neglected. This plex incubation methods (Pileolariini and Janu- approach walls off paleontologists who work ini) have already established in the middle Early predominantly with tubes and rarely calcified Cretaceous, suggesting that the main diversifi- opercula. In non-spirorbin serpulids tube mor- cation of spirorbins should take place before. 296 A.P. Ippolitov, A.V. Rzhavsky

Tube ultrastructures and mineralogy and tigation has not been previously applied to any their potential in decrypting paleontological serpulid genera, and can potentially shed light record. Serpulid tube ultrastructural diversity on the problem of empty tube generic affilia- has a good potential for decrypting their paleon- tion. tological record. It became obvious as a result of Mineralogical investigations, in particular, the early studies (Bohnné Havas, 1981; Bubel et estimating the calcite-aragonite ratio of serpulid al., 1983; Bandel, 1986; ten Hove, Zibrowius, tubes, received little attention. Lowenstam 1986; Zibrowius, ten Hove, 1987) that calcium (1954) has shown that calcium carbonate of carbonate crystals of the tube wall may have a serpulid tubes may be represented by calcite, variety of shapes and sizes, and may be arranged aragonite, or their mixture. The first compre- in different ways. Studies over the last two de- hensive overview of serpulid tube mineralogy cades revealed outstanding ultrastructural diver- was presented by Bornhold and Milliman (1973) sity in serpulid tubes (e.g., Nishi, 1993; Sanfilip- who analyzed over 100 specimens belonging to po, 1998a,b, 2001; Vinn, 2005, 2007, 2008; Vinn 30 species from 15 genera. Their results showed et al., 2008a), which is currently classified into 13 no correlations of mineralogical composition ultrastructural types (Vinn et al., 2008a,b). with temperature, and also no correlations were The idea to evaluate generic affiliation of found with taxonomic groups (genera). More- fossil serpulid species using tube ultrastructures over, calcite-aragonite ratio significantly varied was first proposed by Sanfilippo (1998b). In not only among, but also within species, and Recent forms tube transparency can be a result even within a single tube (Bornhold, Milliman, of certain ultrastructural characters (ten Hove, 1973). Vinn et al. (2008a) has demonstrated Zibrowius, 1986; Ippolitov, Rzhavsky, 2008; some correlations of mineralogy with ultra- Vinn et al., 2008a; Vinn, Kupriyanova, 2011); structural types, but no clear correlations with in one case such tube wall ultrastructure was taxonomy (genera) were found. The most recent included into the diagnosis of species [Pla- comprehensive analysis (Smith et al., 2013) of costegus tridentatus (Fabricius, 1780), see San- both published and new data has shown that filippo, 2003]. Vinn et al. (2008a), who have phylogenetic factor is the most important for analyzed the largest set of tubes scattered among understanding tube mineralogy. Like in case of serpulid genera, concluded that ultrastructure is ultrastructures, mineralogical composition of more likely to be a specific character rather than tubes shows more or less clear correlations with a generic one. This assumption devaluates ultra- large clades of Serpulidae sensu Kupriyanova et structures as a tool for determining generic al. (2009). affinity of fossils. However, some outline of evolutionary interrelations of different ultra- Spirorbin tube ultrastructures and miner- structural types can be provided (e.g., Vinn et alogy. All the ultrastructural and mineralogical al., 2008a; Vinn, Kupriyanova, 2011; Vinn, investigations so far covered mainly non-spirorb- 2013), and together with fossil record analysis, in Serpulidae. Spirorbin ultrastructures were this approach can be used for decrypting the not included in most extensive overview of evolutionary interrelations of major clades (sen- serpulid tubes by Vinn et al. (2008a). The only su Kupriyanova et al., 2009) within Serpulidae. paper focused on Spirorbinae was published by Tube ultrastructures in some serpulids have Ippolitov and Rzhavsky (2008). A list of spirorb- been also shown to have adaptive significance in species with published and figured tube ultra- (Vinn et al., 2008a,b; Tanur et al., 2009; Vinn, structures counts eight Recent species, which Kupriyanova, 2011), but these investigations are not always correctly identified: do not provide any connections to taxonomy for 1. Neodexiospira sp., probably Neodexiospi- the moment. The approach of a systematic anal- ra foraminosa (Bush in Moore et Bush, 1904); ysis of ultrastructural diversity within closely originally determined as Janua steueri (Sterz- related groups of species adopted in this inves- inger, 1909) (see Nishi, 1993, Fig. 1F). Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 297

2. Spirorbis cf. rupestris Gee et Knight- (Vinn et al., 2008a,b), it should be stated that Jones, 1962 (see Weedon, 1994, Fig. 3; in fact spirorbin ultrastructural diversity is comparable it is probably not a true Spirorbis). with that of other serpulids. Both in non-spirorbin 3. Spirorbis spirorbis (Linnaeus, 1758); also serpulids and spirorbins, studies of tube ultra- fossil material (Early Pleistocene; 1.8–1 Ma) structures can potentially become useful for from Mediterranean region was studied (see estimating generic affiliations. Sanfilippo, 1998a, Pl. 2). Mineralogical data on spirorbin tubes are 4. Spirorbis sp. (see Taylor, Vinn, 2006, also scarce. Bornhold and Milliman (1973) Fig. 1D; can be identified only as “Spirorbinae mention two specimens of Spirorbis borealis sp.”). Daudin, 1800 (junior objective synonym of 5. Spirorbis rothlisbergi Knight-Jones, 1978 Spirorbis spirorbis (Linnaeus, 1758)). One of (see Ippolitov, Rzhavsky, 2008, Fig. 1a). them was found to be pure calcitic, while anoth- 6. Protolaeospira (Dextralia) stalagmia er had 10.5% aragonite content. Neither data on Knight-Jones et Walker, 1972 (see Ippolitov, accuracy of the analysis, nor any morphological Rzhavsky, 2008, Fig. 1c). characteristics confirming the determinations 7. Protolaeospira augeneri Vine, 1977 (see are available. Ippolitov, Rzhavsky, 2008, Fig. 1d). 8. Protoleodora uschakovi Knight-Jones, Objectives of study. The aims of the present 1984 (see Ippolitov, Rzhavsky, 2008, Fig. 1b). investigation are 1) to provide comprehensive Nishi (1993, tab. 1) provided crystal mea- descriptions of mineralogy and ultrastructures surements for one more species, “Pileoralia of spirorbin tubes covering as many Recent [sic!] girdis” (probably = ?Pileolaria sp.; name species as possible and 2) to examine potential unknown in literature), but has not accompanied correlations of ultrastructural and mineralogi- them with any description or figure. Five more cal characters with taxonomic groups, tube specimens of Spirorbis spp., without further morphology, as well as with ecological and specification, ranging from Pliocene to Recent, biogeographical patterns. have been only referred to have “fine-grained” The results of our study will form a series of tubes (Taylor, Vinn, 2006). Also, two species of papers, each of them dealing with a tribe of Recent “Spirorbis spp.” (Weedon, 1994) and a Spirorbinae. Tribes will be presented in the fossil species from the Early Santonian (~86 order of growing complexity of their brooding Ma) of UK mentioned as “Spirorbis plana methods (Paralaeospirini → Spirorbini → Cir- (Woodward)” [probably should be referred to ceini → Romanchellini → Januini → Pileolari- Neomicrorbis crenatostriatus subrugosus (Mün- ini), while genera within tribes and species ster in Goldfuss, 1831)] were stated to have within genera will be arranged in alphabetical studied ultrastructures (Taylor, Vinn, 2006); how- order. Conclusions on each tribe, as well as ever, no descriptions or figures were provided. corresponding discussions, will be provided in Most authors found spirorbins to have sim- the relevant parts, while the extended general ple unilayered tubes consisting of ricegrain-like discussion will be published in the last paper of crystals, oriented chaotically. But it also was the series. shown (Ippolitov, Rzhavsky, 2008) that like in serpulids inner and outer tube surfaces are often Tube morphology and terminology strengthened by different types of ultrastruc- tures, providing consolidation of the tube wall Spirorbins live in small tubes coiled into — “dense layers” sensu Vinn and Kupriyanova spirals 1.5–4 (up to 8) mm in diameter, attached (2011). The main conclusion of Ippolitov, to substrate and containing up to 5 coils. Nor- Rzhavsky (2008) was that spirorbin tube ultra- mally the spirals are flat, but distal parts may be structures are not uniform. After the diversity of uncoiled (evolute) and raising above the sub- Recent non-spirorbin serpulids became known strate (Fig. 1C), with overlapping coils, or 298 A.P. Ippolitov, A.V. Rzhavsky

Fig. 1. External morphology of Spirorbinae tubes. A — Neodexiospira alveolata (Zachs, 1933): dextral (anticlockwise) tube with longitudinal keels and alveoli; B — Bushiella (Jugaria) similis (Bush, 1905): sinistral (clockwise) unsculptured tube; C — Bushiella (Jugaria) kofiadii Rzhavsky, 1988: sinistral (clockwise) tube with three longitudinal keels and tube mouth facing upward from substrate; D — Protolaeospira eximia (Bush, 1905): sinistral (clockwise) tube with transverse ridges. Рис. 1. Внешняя морфология трубок спирорбин. A — Neodexiospira alveolata (Zachs, 1933): право- закрученная (против часовой стрелки) трубка с продольными килями и альвеолами; B — Bushiella (Jugaria) similis (Bush, 1905): левозакрученная (по часовой стрелке) неcкульптурированная трубка; C — Bushiella (Jugaria) kofiadii Rzhavsky, 1988: левозакрученная (по часовой стрелке) трубка с тремя продольными килями и приподнятым над субстратом устьем; D — Protolaeospira eximia (Bush, 1905): левозакрученная (по часовой стрелке) трубка с поперечными гребнями. straight and attached to the substrate. Among strate. Most species are known to have only one completely attached forms, tubes may have all coiling direction, but tubes of several Spirorbis the coils well visible or the later coils may partly species may coil in either direction, and all spe- or completely cover the previous ones, resulting cies of Neomicrorbis normally coil in either in hiding the entire spiral by the last coil (see direction. Rarely, some Circeini and Januini (nor- Rzhavsky, 1994, Fig. 1G, J). Coiling direction mally dextral) may have specimens with clock- can be clockwise (sinistral; Fig. 1B–D) or anti- wise coiling, but dextral specimens have never clockwise (dextral; Fig. 1A). To determine the been recorded among typically sinistral species. direction of the coiling, tubes should be ob- Tubes may be unsculptured (Fig. 1B) or served from the upper side, opposite the sub- have external ornamentation (sculpture) on the Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 299 tube surface. Typically it consists of longitudi- tion of growth lines does not correlate with nal (Fig. 1A, C) or transverse (Fig. 1B) ele- appearance of crystals, and thus, cannot be ments. A single major prominent longitudinal interpreted as a character related to ultrastruc- keel or several parallel keels, often termed lon- ture, therefore, we follow Vinn’s suggestion. gitudinal ridges (usually 2–5, but up to 10 and The term “layer” in application to serpulid even more in Neomicrorbis), may be present. tubes needs some clarification. It is not always The keels may either be sharp or obtuse, high or possible to distinguish layers within the wall low, or have the appearance of longitudinal based on different amount of amorphous ce- rows of larger denticles and smaller tubercules. ment, as was proposed by Vinn et al. (2008a: In most cases all keels are equally developed, 643). In such case, multiple contradictive inter- but often certain keels (usually the median one) pretations of layers number become possible, can be better pronounced. Transverse tube or- depending, for example, on the method of study. namentation in spirorbins may be presented by Also, crystal appearance can gradually change regularly spaced transverse collar-like ridges, within a wall (Vinn et al., 2008a; and below), sometimes interpreted as growth stops. Also, in forming slight transitions from one “layer” to some spirorbins tube surface may be completely another. In the present series we use term “lay- or partially pitted by alveoli (Fig. 1A) that er” only for well-delimited longitudinally struc- sometimes completely perforate keels. Attached tural elements, distinguishable by the certain tube parts often produce flattened peripheral shape and/or size of crystals, while in all other flanges that also may contain regularly spaced cases more neutral terms “outer”, “middle” and alveolar structures. “inner part/zone” of the wall/layer are used. Tubes are usually chalky white (opaque), This terminology is consistent with that of rarely they may be completely transparent (vitre- Weedon (1994). ous) or partially transparent (semitransparent) or somewhat transparent, the last state is probably Material and methods caused by the low thickness of the wall. In spirorbins with vitreous tubes the coloured in- The study is based on a collection of spirorb- ner lining of the tube or the body of live speci- in tubes made by A.V. Rzhavsky and deposited mens may be seen through tube walls. The tube in A.N. Severtsov Institute of Ecology and Evo- surface may be rough, more or less smooth, or lution, Russian Academy of Sciences, Moscow smooth with shining (porcellanous) outer layer. (IPEE RAS). Two specimens of Neomicrorbis azoricus were obtained from the collections of Terminology of ultrastructures P.P. Shirshov Institute of Oceanology of Rus- sian Academy of Sciences, Moscow (SIO RAS). We follow the classification of ultrastruc- Although the tubes studied with scanning elec- tures and their terminology developed for Re- tron microscopy (SEM) and analyzed for miner- cent serpulids by Vinn et al. (2008a) and based alogy have been destroyed, conspecific tubes on classification of carbonate ultrastructures by from the same samples are available in the Carter et al. (1990). They distinguish 12 types of collection. Over 750 SEM microphotographs ultrastructures arranged in 1 to 4 wall layers, and 70 X-ray diffraction diagrams were ob- and one additional type was described separate- tained and analyzed, and a number of photo- ly (Vinn et al., 2008b). These types are usually graphs of tubes were taken to illustrate external referred to by abbreviations of their full names. tube morphology. The term “parabolic structure” widely used For the SEM dried tubes were cracked me- in older paleontological literature (= “chevron” chanically and covered with a thin layer of gold structure of Weedon (1994)) was transformed or platinum. We used longitudinal sections run- in Vinn’s papers into “parabolic growth lines” ning along the lateral sides of the tube. This or “parabolic lamellae”. Because the configura- direction of sectioning allows observing para- 300 A.P. Ippolitov, A.V. Rzhavsky bolic growth lines (“parabolic lamellae”, “chev- provide values of absolute intensity (I) of reflec- rons” sensu Weedon, 1994). For most species tion peaks. If the intensities of calcite (Icalc) and/ we studied both external (outside the whorl) and or aragonite (Iarag) major peaks are close to the internal (near the centre of whorl) walls of the background intensity (Ibgr=5–6), the calcula- tube, however, descriptions are primarily based tions of calcite/aragonite ratio for correspond- on longitudinal sections of the external wall, ing sample are unreliable. which are the most informative. In some species Because most spirorbins are small, the quan- tube cross sections were also studied. No spe- tity of powder obtained from a single tube often cial etching techniques were used to prepare falls somewhere around the edge of the diffrac- sections. Although sections are often embedded tometer resolution ability. To improve data re- into epoxide resin with subsequent polishing liability, in most cases we had to analyze calcite- and etching, both literature (Bohnné Havas, aragonite ratios averaged over a set of speci- 1981; Weedon, 1994) and our comparative etch- mens. Yet, for some species the quantity of ing trials using four agents (hydrogen peroxide, available material was insufficient even for such Javel water, formylic acid and acetic acid) kind of analysis, so our mineralogical study showed that thin details of ultrastructure, such covered only about 80% of species studied with as crystal appearance, are better seen in simple SEM. Exact quantity of powder studied in each fractures than in polished etched material. Sec- case differed depending on material availability tions were observed using a CamScan electron for each species, thus affecting reliability of microscope in the Office of Instrumental Ana- analysis for each case. For several species, two lytics of Paleontological Institute of Russian independent samples were taken: one based on Academy of Sciences, Moscow (PIN RAS) and a single specimen, another averaged over sever- a Vega-Tescan microscope in the Electron Mi- al specimens. croscopy Laboratory of IPEE RAS (Moscow). For illustration of tube morphology spirorb- In total, tubes of over 70 species from all 6 ins tubes were photographed with a digital cam- Spirorbinae tribes were studied with SEM, thus, era DFC295 under microscope Leica MZ6 by covering 53% of total Recent spirorbin rich- method of sequential layers. Helicon Focus soft- ness. When possible, we examined several spec- ware was used for merging differently focused imens of each species to assess potential in- images. traspecific variability of ultrastructures. For X-RAY diffraction analysis spirorbin Results tubes pounded into powder were analyzed with an X-ray diffractometer DRON-3M in the labo- Tribe Paralaeospirini Knight-Jones, 1978 ratory of the Geological Faculty of Moscow State University (GF MSU). Signal was ana- Diagnosis. The egg-string is incubated in lyzed in the interval 30–36° 2θ with step 0.1°, the parent’s tube, being neither attached to the containing major peaks of both calcite (34.35° tube wall, nor to the body of a parent; according- 2θ; corresponding spacing between diffracting ly, the only type of operculum throughout life planes d=3.04 A) and aragonite (31.00° and time is an endplate, usually with a talon. Other 31.65 2θ; corresponding spacing between dif- characteristic features are: 1) narrow saw to fracting planes d=3.40 A and d=3.29 A, respec- rasp-shaped thoracic uncini, each starting with tively). Calcite/aragonite ratio was calculated one row of large teeth posteriorly and ending using Ca/Ar main peak intensity ratio, and high with 3 rows of large teeth in front of blunt Mg content of calcite in several cases was esti- anterior peg; 2) abdominal uncini distributed mated visually by the shift of the peak to dolo- asymmetrically: they are absent from the con- mite (3.00–3.01 A), with no further calculations vex side of body, or present only on last chaeti- because of insufficient amount of the material. gers; 3) abdominal chaetae are flat geniculate, To demonstrate the reliability of the data, we pennant-shaped (blade width decreases gradu- Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 301 ally towards tip), usually with a thick projecting Paralaeospira claparedei Caullery et heel; the length of their blade is no longer than Mesnil, 1897 blade length of largest collar chaetae; 4) abdom- Fig. 2A–D. inal companion capillary hooked chaetae may be present only on last abdominal chaetigers; 5) For descriptions see Caullery, Mesnil, 1897: 204, Pl. VIII, fig. 10 (as “Spirorbis (Paralaeospira) claparedei”); larvae are without white attachment glands. Harris, 1969: 142–145, fig. 4 a–l (as “Spirorbis clapare- Remarks. The tribe unconditionally con- dei”). tains the only genus Paralaeospira Caullery et Material examined. Two specimens were Mesnil, 1897. Genera Metalaeospira Pillai, 1970 examined with SEM in longitudinal sections and Eulaeospira Pillai, 1970 initially included (IPEE No. 3/2562, Magellan Strait, shallow in Paralaeospirini (Knight-Jones, Fordy, 1979; water, on Macrocystis fronds). Mineralogy was Knight-Jones P. et al., 1979) incubate embryos analyzed by a single tube from the same sample. in the sac attached to the body, have brush-type Outer tube morphology was illustrated for spec- abdominal chaetae and therefore, belong to the imens from the same sample and from IPEE No. tribe Romanchellini (Knight-Jones P., Knight- 1/2536 (Prince Edward Islands, depth 110 m, on Jones E.W., 1994). bryozoans). Two monotypic genera Anomalorbis Vine, Tube morphology. Tubes are sinistral, pl- 1972 and Crozetospira Rzhavsky, 1997, with anospiral (Fig. 2A) or with overlapping coils yet unknown incubation method, were original- (Fig. 2B), tube mouths may be facing upward ly placed within Paralaeospirini provisionally. from substrate (Fig. 2C). Whorl diameter is up Therefore, only tubes of Paralaeospira are dis- to 2.5 mm. Tube walls are thin and fragile, white cussed here, while tube ultrastructures of Croze- opaque or somewhat transparent, non-porcell- tospira dufresnei Rzhavsky, 1997 will be de- anous or slightly porcellanous. Tube surface is scribed in subsequent papers, among other spirorb- smooth, unsculptured; specimens attached to ins of uncertain tribe attribution. Material on algae may produce peripheral flange (Fig. 2B). Anomalorbis was not available for our study. Tube ultrastructures. Wall is unilayered, Distribution. Mostly south temperate belt with irregularly oriented prismatic (IOP) struc- and Antarctic (Knight-Jones P., Knight-Jones ture. Two studied specimens have slightly dif- E.W., 1984), though P. malardi is known only ferent appearance of crystals in tube wall. One from boreal waters of north-eastern Atlantic demonstrates isometric small crystals 0.5–0.75 (Knight-Jones P., Knight-Jones E.W., 1977; µm long mixed with some cement in inner part Knight-Jones P. et al., 1991). of the wall, gradually turning to slightly elongat- ed angular crystals up to 1–2 µm long and 0.7– Genus Paralaeospira Caullery et Mesnil, 1.2 µm wide in the outer part; total wall width in 1897 the same section is 32–35 µm. A section ob- tained for another specimen (Fig 2D) shows Type species: Spirorbis (Paralaeospira) mostly elongated crystals of 2–3 µm long mixed aggregata Caullery et Mesnil, 1897 with a small amount of cement, except for inner- Diagnosis. Sinistral tubes; margins of collar most zone, where crystals are small and isomet- and thoracic membranes not fused over thoracic ric; corresponding total wall width is 35–40 µm. groove; large collar chaetae bent, with basal fins Crystal shapes are angular in both studied spec- and distal serrated blades without cross-stria- imens. Distinct growth lamellae are absent, but tion; simple limbate and sickle chaetae in 3rd at least one area with unclear orientation of thoracic fascicles; four thoracic chaetigers. elongated crystals along growth lines was ob- Composition. The genus includes 10 spe- served (Fig. 2D). Inner organic lining is thin cies, four of which are covered in the present (not exceeding 1 µm). study. Tube mineralogy. 100% calcite (Icalc.=32) Distribution. As for the tribe. with high Mg content. 302 A.P. Ippolitov, A.V. Rzhavsky

Fig. 2. A–D — Paralaeospira claparedei. A–C — tubes: A — planospiral tube (IPEE No. 3/2562), B — tube with overlapping coils and C — tube with mouth faced upward from substrate (IPEE No. 1/2536); D — longitudinal wall section at the external side of spiral showing IOP ultrastructure, note smaller crystals near the internal side of the wall, probably representing inner layer of oriented prismatic crystals; E–G — Paralaeospira levinseni. E–F — tubes: E — planospiral tube (IPEE No. 1/2398), F — tubes with overlapping coils (IPEE No. 2401); G — longitudinal wall section at the external side of the coil, showing IOP structure. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 303

Distribution. Southern Atlantic and Atlan- No. 2/2401 (Bunger-Hills, Mawson Sea, depth tic sector of Southern Ocean: Magellan Strait 20–50 m, on the sea urchin spines). (Knight-Jones P., Knight-Jones E.W., 1991) Tube morphology. Tubes are sinistral, pl- and Cape Horn (Caullery, Mesnil, 1897), prob- anospiral (Fig. 2E) either with overlapping coils ably Falkland and South Orkney Isles (Knight- (Fig. 2F) or last whorl can be evolute (Vine, Jones P., Knight-Jones E.W., 1984). Southern 1977, Fig. 8a). Whorl diameter is up to 2.5 mm; Indian Ocean: Kerguelen Isles (Harris, 1969); tube walls are thin and fragile, white opaque or Prince Edward and Crozet Isles (Rzhavsky, slightly transparent, with smooth non-porcell- 1998). anous or slightly porcellanous surface; unsculp- Ecology. The species is known from the tured or rarely with vestigial longitudinal keel. shallow water (probably intertidally) up to 110 Dense aggregations are often formed as a result m deep. It lives on brown algae, seaweeds, shell of larval gregarious settlement on adult tubes fragments, and bryozoans. (see Knight-Jones P., Walker, 1972, Fig. 1a, 2a, Remarks. P. claparedei is known only from b; Vine, 1977, Fig. 8a). Tube ultrastructures. Wall is unilayered with several records. Its tube morphology is similar irregularly oriented prismatic (IOP) structure. to that of another rare species from the Southern Crystal average size and appearance is more or Hemisphere, P. patagonica that may be the less uniform throughout wall, but changes slight- same species as P. claparedei (see Remarks for ly from the inner to the outer zones. Crystals in the P. patagonica). inner half of the wall are mostly isometric to slightly elongated (Fig. 2G), small (0.3–1 µm). Paralaeospira levinseni Caullery et Mesnil, Outer half of the wall contains relatively more 1897 elongated larger crystals ~1–1.2 µm, rarely up Fig. 2E–G. to 2 µm long; corresponding wall thickness is 20 µm. No distinct growth lamellae are visible. For descriptions see Caullery, Mesnil, 1897: 204, Pl. Inner organic lining is thin (0.5 µm or less). VIII, fig. 14 (as “Spirorbis (Paralaeospira) levinseni”); Knight-Jones P., Walker, 1972: 33–35, Fig. 1 a–n, 2 a, b; Tube mineralogy. 100% calcite (Icalc.=115) Vine, 1977: 17–20, Fig. 2 e, 6 c, 8 a–j. with high Mg content. Material examined. Two specimens were Distribution. The species is widely distrib- examined with SEM in longitudinal sections uted in the Southern Hemisphere. Known (IPEE No. 1/2398, South Georgia Island, upper throughout the South American coast from Peru sublittoral zone, on the Macrocystis thallus). in the Pacific to Uruguay in Atlantic; off many Mineralogical composition was analyzed in one islands in Southern, South Atlantic, and South sample averaged over 3 tubes from the same Indian Oceans; south coasts of Africa and Aus- sample. Outer tube morphology illustrated us- tralia, New Zealand and Antarctica coasts ing specimens from IPEE No. 1/2398, and IPEE (Knight-Jones P., Knight-Jones E.W., 1984).

Abbreviations: os — outer surface, is — inner surface, pf — peripheral flange. Large arrow indicates tube growth direction. Рис. 2. A–D — Paralaeospira claparedei. A–C — трубки: A — планоспиральная трубка (IPEE No. 3/ 2562), B — трубка с налегающими оборотами, C — трубка с устьем, приподнятым над субстратом (IPEE No. 1/2536); D — продольное сечение стенки трубки с внешней стороны спирали, демонстри- рующее ультраструктуру из хаотически ориентированных призматических кристаллов; заметно, что возле внутренней стороны стенки кристаллы имеют более мелкий размер, возможно, они представ- ляют внутренний слой из призматических кристаллов, ориентированных более-менее параллельно поверхности; E–G — Paralaeospira levinseni. E–F — трубки: E — планоспиральная трубка (IPEE No. 1/2398), F — трубки с налегающими оборотами (IPEE No. 2401); G — продольное сечение стенки на внешней стороне оборота, демонстрирующее структуру из хаотически ориентированных призмати- ческих кристаллов. Условные обозначения: os — наружная поверхность, is — внутренняя поверхность, pf — периферийный фланг. Большая стрелка показывает направление роста трубки. 304 A.P. Ippolitov, A.V. Rzhavsky

Ecology. The species lives from the intertid- µm long (Fig. 3E). Indistinct growth lamellae al zone up to about 50 m deep, where it occupies marked by some difference in amount of cement stones, algae, ascidians, other spirorbin tubes, along smallest discernible growth lines can be and sea urchin spines. observed in all sections. Inner organic lining is thick, about 5–6 µm (Fig. 3C). Paralaeospira malardi Caullery et Mesnil, Tube mineralogy. Not studied due to insuf- 1897 ficient material. Fig. 3A–F. Distribution. This is the only Paralaeospira known from the Northern Hemisphere. It is For descriptions see Caullery, Mesnil, 1897: 205, Pl. recorded from north-east Atlantic off the Brit- VIII, fig. 11a, b (as “Spirorbis (Paralaeospira) malardi”); Knight-Jones P., Knight-Jones E.W., 1977: 474–476, Fig. ish, Irish, French and Spanish coasts (Knight- 7 A–H. Jones P., Knight-Jones E.W., 1977). Material examined. Two specimens were Ecology. The species lives from the lower examined with SEM in longitudinal sections intertidal zone to the depths of about 25 m, (IPEE No. 1/2558, English Channel, depth 1–5 where it usually occupies stones, sometimes m, on stones). Outer tube morphology was illus- mollusk shells and decapod carapaces, rarely trated for a specimen from the same sample. can be found on algae. Tube morphology. Tubes are sinistral, pl- anospiral; up to 2.0 mm in whorl diameter; Paralaeospira patagonica Caullery et white opaque with distinctly porcellanous Mesnil, 1897 smooth surface, bearing an obtuse median keel Fig. 4A–I. often terminating as a tooth-like projection over tube mouth (Fig. 2A); juveniles usually lack For descriptions see Caullery, Mesnil, 1897: 205– 206, Pl. VIII, fig. 12 (as “Spirorbis (Paralaeospira) patag- keel. Tube aggregations are unknown. onicus”); Harris, 1969: 162, fig. 15a–l (as “Spirorbis Tube ultrastructures. Tube wall is visually patagonicus”). unilayered with irregularly oriented prismatic Material examined. Two specimens were (IOP) structure consisting of two distinct zones. examined with SEM in longitudinal sections Outer and middle parts of the wall are made of (IPEE No. 2/2575, Swakopmund, Namibia, low isometric crystals mixed with cement (Fig. 3B). intertidal zone, on undersides of stones). Miner- Crystal size range is 0.5–3 µm, typically about alogical composition was analyzed by a single 0.5–1 µm; corresponding wall width is 40 µm tube from the same sample. Outer tube mor- (Fig. 3C, D). Crystals of the innermost wall part phology was illustrated for specimens from the form a thin layer, often not clearly visible in same sample and from IPEE No. 1/2561 (Ker- longitudinal sections and consisting of acicular guelen Island, Southern Indian Ocean, on algae, crystals 3–5 µm long and 0.5–0.8 µm wide, depth unknown). lying more or less parallel to the lumen with no Tube morphology. Tubes are sinistral, pl- further orientation. A longitudinal section made anospiral (Fig 4A, B) or often with overlapping near the tube base shows elongated acicular coils (Fig. 4C); up to 2.5 mm in whorl diameter; crystals similar to those of the innermost zone thin-walled, fragile, white opaque; with smooth by shape, but sometimes slightly longer, up to 5 non-porcellanous or slightly porcellanous sur-

Рис. 3. Paralaeospira malardi: A — трубка с хорошо развитым серединным килем и блестящей фарфоровидной поверхностью; B–E — ультраструктуры трубок, экземпляр № 1 [B — продольное сечение наружной стороны оборота; C — внутренняя органическая мембрана трубки, также заметны

прилипшие к ней призматические кристаллы CaCO3; D — внутренняя поверхность трубки (органи- ческая мембрана удалена), демонстрирующая уплощенную поверхность с удлиненными кристалла- ми); E — кристаллы непосредственно под органической мембраной]; F — экземпляр № 2, продоль- ное сечение наружной части последнего оборота). Условные обозначения: os — наружная поверхность, is — внутренняя поверхность, iol — внутренняя органи- ческая мембрана. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 305

Fig. 3. Paralaeospira malardi: A — tube with well-developed median keel and porcellanous surface; B–E — tube ultrastructures. Specimen 1 [B — longitudinal section of the external side of the coil; C — inner organic lining, also showing embedded prismatic CaCO3 crystals; D — inner surface of the tube (organic layer removed) showing flattened surface made of elongated crystals; E — crystals near the lumen]; F — specimen 2, longitudinal section of the external side of the last whorl. Abbreviations: os — outer surface, is — inner surface, iol — inner organic lining. 306 A.P. Ippolitov, A.V. Rzhavsky

Fig. 4. Paralaeospira patagonica. A–C — tubes: A — planospiral tube with a single vestigial keel and pronounced growth lines, B — planospiral tube with two vestigial keels (IPEE No. 1/2561), C — aggregation of unsculptured tubes with overlapping coils (IPEE No. 2/2575); D–I — tube ultrastructures: D — general view of longitudinal section near the tube mouth, E–G — details of different parts of the wall, H — contact of the mineral wall with inner organic lining, note the adhesion of calcite crystals to the organic lining, I — tube surface just under the inner organic lining. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 307 face (Fig. 4C), unsculptured, or bearing one or Remarks. P. patagonica is known only by two vestigial keels (Fig. 4A, B); dense aggrega- several records and is similar in external tube tions are often formed (Fig. 4C). morphology as well as in opercular and chaetal Tube ultrastructures. Wall is unilayered, structure to another rare species from Southern with IOP ultrastructure represented by slightly Hemisphere, P. claparedei, which in our opin- elongated to distinctly elongated loosely packed ion may be a synonym of the P. patagonica. crystals 1–3 µm long; corresponding wall width General appearance of wall ultrastructures in is 70 µm (Fig. 4D). Crystals are gradually be- these two species also shows high similarity, coming less elongated and more isometric (Fig. like in all studied Paralaeospirini. Although in 4G) towards external tube surface. Middle part P. claparedei we have not observed an inner of the wall contains numerous smaller isometric layer made of oriented elongated crystals, sim- crystals of uniform size and interspersed among ilar to that found in P. patagonica, this may be larger elongated crystals (Fig. 4E, F). Innermost due to scarcity of studied material. Additional part of the wall is represented by acicular crys- morphological studies are needed to clarify the relationship between these two species; here we tals (4–6 µm long and ~0.5 µm wide) lying consider them both valid. parallel to the lumen (Fig. 4H, I). Growth lamel- lae are distinct and marked by variations of Tube morphology of species not crystal size. Parabolic lamellae symmetrical, their axes are located centrally in the wall. Inner covered with the SEM study organic lining is 3–6 µm wide. External tube morphology markedly varies Tube mineralogy. 100% calcite (I =73). calc among six species of Paralaeospira not cov- Calcite has high Mg content (main peak at 34.61 ered with SEM study. Two of these species, P. 2θ). pseudotenuis Rzhavsky, 1997 and P. sicula Distribution. The species is known through Knight-Jones et Knight-Jones, 1994, were ex- the south coast of Africa from Namibia to Port amined by the second author. General morphol- Elisabeth, Republic of South Africa; off the ogy of P. pseudotenuis tube is similar to those of south of Chile and some islands of South Atlan- P. claparedei, P. levinseni, and P. patagonica tic and Atlantic sector of Southern Ocean (Fig. 5A, B). Tubes of P. sicula are usually (Knight-Jones P., Knight-Jones E.W., 1984); evolute and have quadrangular cross-section with off some islands of Southern Indian Ocean very characteristic sharp keels (Fig. 5C, D). (Rzhavsky, 1998). Tube morphology of other species of Para- Ecology. This is a shallow water species laeospira is known from literature only. P. mo- living in the intertidal and upper sublittoral nacantha (Augener, 1923) has tubes similar to zones, but exact bathymetric data are absent. It those of P. claparedei, P. levinseni, and P. occupies bryozoans, algae, and undersides of patagonica and often produce aggregations (Fig. stones. 5E). P. parallela Vine, 1977, like P. malardi, is

Abbreviations: os — outer surface, is — inner surface, iol — inner organic lining. Large arrow indicates the direction of tube growth. Рис. 4. Paralaeospira patagonica. A–C — трубки: A — планоспиральная трубка с одним зачаточным продольным килем и выраженными линиями нарастания, B — планоспиральная трубка с двумя зачаточными продольными килями (IPEE № 1/2561), C — агрегация нескульптурированных трубок с налегающими оборотами (IPEE № 2/2575); D–I — ультраструктуры трубок: D — общий вид продольного сечения близ устья трубки; E–G — различные участки стенки, более крупно, H — контактовая зона стенки и внутренней органической мембраны, хорошо заметно прилипание крис- таллов кальцита к мембране, I — внутренняя поверхность трубки и облик кристаллов непосредствен- но под мембраной. Условные обозначения: os — наружная поверхность, is — внутренняя поверхность, iol — внутренняя органи- ческая мембрана. Большая стрелка показывает направление роста трубки. 308 A.P. Ippolitov, A.V. Rzhavsky

Fig. 5. Tubes of Paralaeospirini species not covered in the present study. A, B — Paralaeospira pseudotenuis (from Rzhavsky, 1997); C, D — P. sicula (from Knight-Jones, Knight-Jones, 1994); E — P. monacantha (from Vine, 1977); F — P. parallela (from Vine, 1977); G — P. aggregata (from Harris, 1969); H — P. adeonella (from Day, 1963). Рис. 5. Морфологическое разнообразие трубок представителей Paralaeospirini, которые не изучались авторами в ходе настоящего исследования. A, B — Paralaeospira pseudotenuis (из Rzhavsky, 1997); C, D — P. sicula (из Knight-Jones, Knight-Jones, 1994); E — P. monacantha (из Vine, 1977); F — P. parallela (из Vine, 1977); G — P. aggregata (из Harris, 1969); H — P. adeonella (из Day, 1963). always solitary and has planospiral hard tubes dense aggregations (Fig. 5G). P. adeonella (Day, that are, however, non-porcellanous and lack 1963) known only from its original description, longitudinal keel(s). The characteristic feature has thick-walled, hard and vitreous tubes with of the P. parallela tube is the mouth completely well-pronounced transverse ridges (Fig. 5H). covering the preceding whorl (Fig. 5F). P. ag- Similar tubes are not known for other Paralae- gregata (Caullery et Mesnil, 1897), like P. ospira spp. and are more common in the genus malardi, has porcellanous tubes, but unlike P. Protolaeospira from tribe Romanchellini. Un- malardi, it lacks any longitudinal sculpture. fortunately, data on incubation method and mor- Besides, tubes of P. aggregata are never plano- phology of abdominal chaetae that could have spiral, coils always overlap and the last coil is helped to clarify systematic position of P. ade- usually straightened. This species always forms onella, were not provided. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 309

Discussion ular crystals (length up to 5 µm, width 0.3–0.5 µm), lying parallel to the lumen with no further Patterns and variations. Although three of orientation. A similar thin layer built of acicular the four species described herein have similar crystals was also observed for the non-spirorbin tube ultrastructures, variability in tube mor- serpulid Ficopomatus enigmaticus (Fauvel, phology among all species of Paralaeospira is 1923) by Aliani et al. (1995). Such a layer was very high. The only stable characters are the not mentioned for any species studied by Vinn coiling direction (always sinistral) and the ab- et al. (2008a), probably due to different meth- sence of or small number of keels (usually one, ods of sample preparation, which always in- rarely two). Mineralogical tube composition in cluded treating by aggressive agents. The nature all three studied Paralaeospira species was of this “layer” is probably mechanical arrange- purely calcitic, and all studied species had the ment of elongated rice grain-shaped crystals same ultrastructural type (IOP) composed of near the lumen during the tube formation, and slightly elongated to isometric angular crystals therefore, its presence is not indicative of close lying loosely with no clear orientation of their phylogenetic relationship. The presence of in- long axes (Table 2). ner layer with acicular crystals still cannot be P. malardi shows distinct characteristics excluded for two other species of Paralaeospi- (wall consisting mostly of isometric crystals ra (P. levinseni and P. claparedei), but this with high content of cement, probably of organ- needs to be clarified with new material. ic nature), allowing its recognition among stud- ied Paralaeospira spp. by ultrastructure only. Comparison with other Serpulidae. The Tube morphology of this species also differs unilayered IOP walls found in Paralaeospira from those of other studied species by being are very common among non-spirorbin ser- more thick-walled, always planospiral, white pulids (Vinn et al., 2008a), and therefore, ultra- opaque with distinctly porcellanous surface, structures are not diagnostic. It is easy to distin- and bearing an obtuse median longitudinal keel guish Paralaeospira from all these taxa by that often terminates as a tooth-like projection external morphology, in particular, clockwise over the mouth. Opaque tube appearance is of P. tube coiling combined with small size. Detailed malardi is probably the result of high content of comparisons with other spirorbin tribes will be cement, which is more abundant, than in other provided in the subsequent parts of the present studied species. Other examined species of series. Paralaeospira are characterized by relatively thin-walled tubes, sometimes even semi-trans- Phylogenetic significance. Unilayered tube parent, with non-porcellanous or slightly por- with IOP ultrastructure of Paralaeospira is very cellanous surfaces; coiling can vary from plano- similar to IOP ultrastructures described for ser- spiral to overlapping, or last coil can even be pulids of “clade B” sensu Kupriyanova et al. evolute; longitudinal keel, if present, is vesti- (2009). This clade includes genera such as gial. Additionally, all these species may form Filograna, Salmacina, Protis, Vermiliopsis, aggregations, whereas P. malardi is always sol- Metavermilia, Protula, and Chitinopoma. These itary. P. malardi is also isolated biogeographi- genera form a sister-group to monophyletic cally as it is the only species of the genus spirorbins (Kupriyanova et al., 2006, 2009). Paralaeospira known from the Northern Hemi- Given that in many spirorbins ultrastructures sphere, while others are restricted to the South- appear more derived than those of Paralaeospiri- ern Hemisphere. Nevertheless, general appear- ni (Ippolitov, Rzhavsky, 2008), the hypothesis ance of tube ultrastructures is still very similar that Paralaeospirini having simplest method of among all studied Paralaeospirini. embryos incubation is the most primitive spirorb- Inner organic lining in P. malardi and P. in group is well supported. Therefore, our data patagonica is underlain by a thin layer of acic- confirm a closer relationship of primitive spirorb- 310 A.P. Ippolitov, A.V. Rzhavsky . кальцит content content Cement Cement ; calc— no low no low no medium no low no low no low layer layer inner inner Dense арагонит m) µ IOP IOP IOP IOP 1–1.2 lumen) lumen) lumen) : arag — : arag Main layer layer Main crystal and 1–3 (5 near near 1–3 (5 length ( length 1–2 (rarely 3) 3) 1–2 (rarely 1–3 (4–6 near near 1–3 (4–6 layer layer outer outer Dense обозначения

Mg Mg Условные in calc content content (%) (%) calc arag/ 0/100 high 0/100 high no 0/100 high 0/100 high no 0/100 high no no data no data no data no content content Paralaeospirini. видов

smooth, smooth, distinctly distinctly or slightly or slightly or slightly or slightly or slightly porcellanous porcellanous porcellanous porcellanous porcellanous porcellanous porcellanous porcellanous porcellanous smooth, non- smooth, smooth, non- smooth, non- smooth, изученных

трубок

opaque opaque opaque or or opaque opaque or or opaque or opaque somewhat somewhat somewhat somewhat somewhat Table 2. Main tube characters for studied Paralaeospirini. Abbreviations: arag — aragonite; calc calcite. transparent transparent transparent Transparency Surface строения

External morphology External morphology Mineralogy Ultrastructures 1 0–1 0–2 keels черты

median distinct distinct vestigial vestigial vestigial Longitudinal Longitudinal Основные 2.5 0 2.5 2.0 2.5 coil coil Max. Max. (mm) 2. diameter Таблица Species P. claparedei P. claparedei P. levinseni P. malardi P. patagonica Tube morphology, ultrastructures and mineralogy in recent Spirorbinae. I. 311 ins to “clade B”, rather than to other serpulids. Oceanology, Russian Academy of Sciences and However, tubes belonging to the listed genera of the Australian Museum, Sydney, Australia. We “clade B” are characterized by predominantly are also grateful to numerous collectors of the aragonite mineralogy with only little calcite examined materials. The investigation was sup- (Bornhold, Milliman, 1973; Vinn et al., 2008a; ported by the RFBR grant No. 14-05-31413 and Smith et al., 2013). The only species that may RAS Presidium Program No. 28. have calcitic tubes is Filograna implexa (Ber- keley, 1835) (see discussion in Vinn et al., References 2008a: 646). Aragonitic mineralogy of serpulid tubes is Aliani S., Bianchi C.N., de Asmundis C., Meloni R. 1995. interpreted as the most ancient (Vinn, Mutvei, Scanning electron microscope observations on the 2009) according to the well-accepted hypothe- tube of the reef-forming serpulid Ficopomatus enig- maticus (Annelida, Polychaeta) // Bollettino di Zoolo- sis that seawater chemical environment of Late gia. Vol.62. No.4. P.363–367. – Early Jurassic interval, when Augener H. 1923. Polychaeten von den Auckland- und true serpulids first appeared in paleontological Campbell-Inseln // Videnskabelige Meddelelser fra record, was more suitable for aragonite than for Dansk naturhistorisk Forening i København. Vol.75. S.1–115. calcite precipitation. In frame of this hypothe- Bandel K. 1986. The reconstruction of “Hyolithes kingi” sis, first spirorbins, which appear later in the as worm from the of Jordan // “calcitic” seas of the Late Jurassic – Early Mitteilungen aus dem Geologisch-Paläontologischen Cretaceous, should have calcitic tubes. This Institut der Universität Hamburg. H.61. S.35–101. agrees with plesiomorphy of Paralaeospirini Berkeley M.J. 1835. Observations upon the Dentalium subulatum of Deshayes // Zoological Journal (Lon- inferred from the simplest incubation method don). Vol.5. No.20. P.424–427. among Spirorbinae. However, why aragonitic Bohnné Havas M. 1981. A Ditrupa cormea (L.) és konver- serpulids should preserve their mineralogy gens formáinak szelekciója scanning elektronmik- through the “calcitic” epoch, as well as why roszkóppal // Évi Jelentése a Magyar Állami Földtani Intézet. Az. 1979. Évről. P.387–415. calcitic serpulids would not switch their miner- Bornhold B.D., Milliman J.D. 1973. Generic and environ- alogy to aragonite according to Recent environ- mental control of carbonate mineralogy in serpulid ments, has no good explanation now. () tubes // Journal of Geology. Vol.81. No.3. P.363–373. Bubel A., Stephens R.M., Fenn R.H., Feith P. 1983. An Acknowledgements. We thank L.T. Pro- electron microscope, X-ray diffraction and amino tasevich, A.V. Kravtsev and R.A. Rakitov (PIN acid analyses study of the opercular filament cuticle, RAS), N.N. Surovenkova (IPEE RAS) and V.L. calcareous opercular plate and habitation tube of Kosorukov (GF MSU) for their kind help with Pomatoceros lamarckii Quatrefages (Polychaeta: Ser- pulidae) // Comparative Biochemistry and Physiolo- technical part of the study. We are grateful to gy. Vol.74B. P.837–850. E.K. Kupriyanova (the Australian Museum, Burchette T.P., Riding R. 1977. Attached vermiform gas- Sydney, Australia), who reviewed the manu- tropods in Carboniferous marginal marine stromato- script and provided invaluable remarks and sug- lites and biostromes // Lethaia. Vol.10. Iss.1. P.17–28. Bush K. 1905. Tubicolous of the tribes Sabellides gestions, greatly improving the paper. We also and Serpulides from the Pacific Ocean // Harriman thank specialists and Institutions who donated Alaska Expedition. Vol.12. P.169–355. materials to the collection of A.V. Rzhavsky. Carter J.G., Bandel K., de Buffrénil V., Carlson S.J., These are late Phyllis and Wyn Knight-Joneses Castanet J., Crenshaw M.A., Dalingwater J.E., Fran- (University of Wales, Swansea, UK); H. Zi- cillion-Vieillot H., Géradie J., Meunier F.J., Mutvei H., de Riqlès A., Sire J.Y., Smith A.B., Wendt J., browius (formerly Station Marine d’Endoume, Williams A., Zylberberg L. 1990. Glossary of Skeletal Marseille, France); Zoological Institute of Rus- Biomineralization // Carter J.G. (ed.). Skeletal Biom- sian Academy of Sciences, Saint-Petersburg, ineralization: Patterns, Processes and Evolutionary Russia; A. V. Zhirmunsky Institute of Marine Trends. Short Course in Geology. Vol.5. Pt.2. P.609– 671. Biology of Far Eastern Branch of Russian Acad- Caullery M., Mesnil F. 1897. Études sur la morphologie emy of Sciences; P.P. Shirshov Institute of comparée et la phylogénie des espèces chez les 312 A.P. Ippolitov, A.V. Rzhavsky

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